Skip to main content
Log in

A search for Y-chromosomal species-specific markers and their use for hybridization analysis in ground squirrels (Spermophilus: Rodentia, sciuridae)

  • Animal Genetics
  • Published:
Russian Journal of Genetics Aims and scope Submit manuscript

Abstract

In four ground squirrel species from the Volga region—yellow (Spermophilus fulvus), russet (S. major), little (S. pygmaeus), and speckled (S. suslicus)—four hybridization variants (major/fulvus, major/pygmaeus, major/suslicus, and pygmaeus/suslicus) have been reliably described. Earlier we have shown that populations of S. major from the Volga region were characterized by wide introgression of mtDNA from S. fulvus and S. pygmaeus, which probably, resulted from ancient hybridization [5]. In this study, the same populations were used to analyze the introgression of the Y chromosome, which (unlike mtDNA) is paternally inherited. Three genes, ZfY, SRY, and SmcY were tested as Y-chromosomal candidate markers. It was demonstrated that Y chromosome of ground squirrels lacked the ZfY gene, while its homologous structure, ZfY(X), was presumably linked to the X chromosome. The SRY region examined was rather conservative. In particular, the sequences determined in S. major and S. fulvus were identical, while three out of four substitutions found in S. pygmaeus were located in the coding region. The SmcY gene was found to be the most suitable marker, providing distinguishing of all of the four ground squirrel species by nine nucleotide substitutions. Introgression at the Y chromosome was observed only in two cases: in one S. major individual (out of 51 phenotypically pure animals) caught in the major/fulvus sympatry zone, and in four (one litter) out of fourteen S. fulvus individuals caught in close vicinity of the sympatry zone of these two species. Among 28 S. pymaeus and 9 S. suslicus individuals, no foreign SmcY genes were detected. Two colonies of the “hybrid swarm” type were examined with eight major/suslicus hybrids analyzed in the first and seventeen major/fulvus hybrids in the second colony. The prevalence of the S. major paternal lineages was observed in both colonies (87.5 and 82.4%, respectively). The data obtained suggest that compared to wide mtDNA introgression, introgression of Y chromosome in the Volga region ground squirrels is statistically significantly less frequent event.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Bazhanov, V.S., Ground Squirrel Hybrids (to the Problem of Interspecific Hybridization in Nature), Dokl. Akad. Nauk SSSR, 1944, vol. 12, no. 7, pp. 321–322.

    Google Scholar 

  2. Denisov, V.P., On Hybridization between Species of the Genus Citellus Oken, Zool. Zh., 1963, vol. 42, no. 12, pp. 1887–1889.

    Google Scholar 

  3. Formozov, N.A. and Nikol’skii, A.A., Sound Signals in the Hybrid of the Russet and Little Ground Squirrels (Citellus major × C. pygmaeus), Vestn. Mosk. Univ., Ser. 16: Biol., 1986, no. 4, pp. 3–8.

  4. Ermakov, O.A., Russet and Little Ground Squirrels in the Volga Region: Their Distribution and Relationships, Extended Abstract of Cand. Sci. (Biol.) Dissertation, Moscow: Mos. State Univ., 1996.

    Google Scholar 

  5. Ermakov, O.A., Surin, V.L., Titov, S.V., et al., A Molecular Genetic Study of Hybridization in Four Species of Ground Squirrels (Spermophilus: Rodentia, Sciuridae), Rus. J. Genet., 2002, vol. 38, no. 7, pp. 796–809.

    Article  CAS  Google Scholar 

  6. Ognev, S.I., Zveri SSSR i prilezhashchikh stran. Gryzuny (Mammals of the Soviet Union and Adjacent Countries: Rodents), Moscow: Akad. Nauk SSSR, 1947, vol. 5.

    Google Scholar 

  7. Ermakov, O.A., Titov, S.V., Surin, V.L., and Formozov, N.A., To the Problem of Hybrids between Russet and Yellow Ground Squirrels, Sistematika, filogeniya i paleontologiya melkikh mlekopitayushchikh: Materialy dokl. Mezhdunar. konf., posvyashchennoi 90-letiyu prof. I.M. Gromova (Systematics, Phylogeny and Paleontology of Small Mammals: Proc. Int. Conf. to the 90th Anniversary of Prof. I.M. Gromov), St. Petersburg, 2003, pp. 82–85.

  8. Titov, S.V., Ermakov, O.A., Surin, V.L., et al., Molecular Genetic Diagnosis of Russet and Yellow Ground Squirrels from a Mixed Colony, Sbornik tez. Mezhdunar. soveshch. “Mlekopitayushchie kak komponent aridnykh ekosistem (resursy, fauna, ekologiya, meditsinskoe znachenie i okhrana)” (Proc. Int. Conf. “Mammals As a Component of Arid Ecosystems (Resources, Fauna, Ecology, Medical Significance and Preservation)), Moscow: IPEE, 2004, pp. 149–150.

    Google Scholar 

  9. Titov, S.V., Ermakov, O.A., Surin, V.L., et al., Molecular Genetic and Bioacoustic Diagnosis of Russet (Spermophilus major) and Yellow (S. fulvus) Ground Squirrels from Mixed Colony, Byul. Mosk. O-va Ispyt. Prir., Otd. Biol., 2005, vol. 110, no. 4, pp. 72–77.

    Google Scholar 

  10. Titov, S.V., Relationships between Speckled and Russet Ground Squirrels in a Recent Sympatric Zone, Extended Abstract of Cand. Sci. (Biol.) Dissertation, Moscow: Mos. State Univ., 1999.

    Google Scholar 

  11. Ermakov, O., Titov, S., and Bystrakova, N., Interspecific Hybridization in Mammals: A Case of Souslics, Spermophilus major and S. suslicus, Int. Conf. “Evolution, Genetics, Ecology and Biodiversity”: Abstracts, Vladivostok, 2001, p. 52.

  12. Denisov, V.P., Relationships of Major and Speckled Ground Squirrels at the Boundary of Their Ranges, Zool. Zh., 1961, vol. 40, no. 7, pp. 1079–1085.

    Google Scholar 

  13. Ermakov, O.A., Titov, S.V., and Bystrakova, N.V., Data on the Current State of the Boundary Region between the Ranges of Little (Spermophilus pygameus Pallas, 1778) and Speckled (S. suslicus Güldenstaedt, 1770) Ground Squirrels in the Volga Region, Bioresursy i bioraznoobrazie ekosistem Povolzh’ya: proshloe, nastoyashchee, budushchee. Materialy Mezhdunar. soveshch., posvyashchennogo 10-letiyu Sarat. fil. In-ta problem ekologii i evolyutsii im. A.N. Severtsova RAN (Bioresources and Biodiversity of Ecosystems of the Volga Region: Past, Present and Future: Proc. Int. Conf. to the 10th Anniversary of the Saratov Branch of the Severtsov Institute of the Problems of Ecology and Evolution, Russian Academy of Sciences), Saratov: Saratov. Gos. Univ., 2005, pp. 153–154.

    Google Scholar 

  14. Bystrakova, N.V., Ermakov, O.A., and Titov, S.V., Chromosome Trip in the Middle Don Region, Vestn. Vseros. O-va Genet. Selekts., 2005, vol. 9, no. 1, pp. 67–69.

    Google Scholar 

  15. Hoffmann, R.S., Anderson, C.G., Thorington, R.W., and Heaney, L.R., Family Sciuridae, Mammal Species of the World: A Taxonomic and Geographic Reference, Wilson, D.E. and Reeder, D.-A.M., Eds., Washington: Smithsonian Inst. Press, 1993, pp. 419–465.

    Google Scholar 

  16. Arrigi, F.E., Bergendahl, G., and Mandel, M., Isolation and Characterization of DNA from Fixed Cells and Tissues, Exp. Cell Res., 1968, no. 50, pp. 47–53.

  17. Vorontsov, N.N. and Lyapunova, E.A., Chromosomes of Palearctic Ground Squirrels (Citellus, Marmotinae, Sciuridae, Rodentia), Mlekopitayushchie (evolyutsiya, kariologiya, sistematika, faunistika): Materialy 2-go Vses. soveshch. po mlekopitayushchim (Mammals (Evolution, Karyology, Systematics, Faunistics): Proc. 2nd All-Russian Conf. on Mammals), Novosibirsk: Sib. Otd. Akad. Nauk SSSR, 1969, pp. 41–47.

    Google Scholar 

  18. Graves, J.A.M., The Origin and Function of the Mammalian Y Chromosome and Y-Borne Genes—An Evolving Understanding, BioEssays, 1995, vol. 17, pp. 311–320.

    Article  PubMed  CAS  Google Scholar 

  19. Graves, J.A.M., The Rise and Fall of SRY, Trends Genet., 2002, vol. 18, pp. 259–264.

    CAS  Google Scholar 

  20. Pamilo, P. and Bianchi, N.O., Evolution of the ZfX and ZfY Genes: Rates and Interdependence between the Genes, Mol. Biol. Evol., 1993, vol. 10, pp. 271–281.

    PubMed  CAS  Google Scholar 

  21. Agulnik, A.I., Bishop, C.E., Lerner, J.L., et al., Analysis of Mutation Rates in the SMCY/SMCX Genes Shows that Mammalian Evolution Is Male Driven, Mamm. Genome, 1997, vol. 8, pp. 134–138.

    Article  PubMed  CAS  Google Scholar 

  22. Panov, E.N., Gibridizatsiya i etologicheskaya izolyatsiya u ptits (Hybridization and Ethological Isolation in Birds), Moscow: Nauka, 1989.

    Google Scholar 

  23. Funk, D.J. and Omland, K.E., Species-Level Paraphyly and Polyphyly: Frequency, Causes, and Consequences, with Insights from Animal Mitochondrial DNA, Annu. Rev. Ecol., Evol. Syst., 2003, vol. 34, pp. 397–423.

    Article  Google Scholar 

  24. Jaarola, M., Tegelstrom, H., and Fredga, K., A Contact Zone with Noncoincident Clines for Sex-Specific Markers in the Field Vole (Microtus agrestis), Evolution, 1997, vol. 51, pp. 241–249.

    Google Scholar 

  25. Ferris, S.D., Sage, R.D., Huang, C.-H., et al., Flow Mitochondrial DNA across a Species Boundary, Proc. Nat. Acad. Sci. USA, 1983, vol. 80, pp. 2290–2294.

    PubMed  CAS  Google Scholar 

  26. Gyllenstein, U. and Wilson, A.C., Interspecific Mitochondrial DNA Transfer and the Colonization of Scandinavia by Mice, Genet. Res., 1987, vol. 49, pp. 25–29.

    Google Scholar 

  27. Vanderberghe, F., Dod, B., Boursot, P., et al., Absence of Y-Chromosome Introgression across the Hybrid Zone between Mus musculus domesticus and Mus musculus musculus, Genet. Res., 1986, vol. 48, pp. 191–197.

    Google Scholar 

  28. Boissinot, S. and Boursot, P., Discordant Phylogeographic Patterns between the Y Chromosome and Mitochondrial DNA in the House Mouse: Selection of the Y Chromosome?, Genetics, 1997, vol. 146, pp. 1019–1034.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Original Russian Text © O.A. Ermakov, V.L. Surin, S.V. Titov, S.S. Zborovsky, N.A. Formozov, 2006, published in Genetika, 2006, Vol. 42, No. 4, pp. 538–548.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ermakov, O.A., Surin, V.L., Titov, S.V. et al. A search for Y-chromosomal species-specific markers and their use for hybridization analysis in ground squirrels (Spermophilus: Rodentia, sciuridae). Russ J Genet 42, 429–438 (2006). https://doi.org/10.1134/S1022795406040107

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1022795406040107

Keywords

Navigation